Crop Protection 77 (2015) 38e44 Contents lists available at ScienceDirect Crop Protection journal homepage: www.elsevier.com/locate/cropro Flea beetles (Coleoptera: Chrysomelidae, Alticinae) in Bt- (MON810) and near isogenic maize stands: Species composition and activity densities in Hungarian fields * Agnes Szen asi a, , Viktor Marko b a Plant Protection Institute, Faculty of Agriculture and Environmental Sciences, Szent Istvan University 2100 God€ oll€ oP} ater K. str. 1, Hungary b Department of Entomology, Faculty of Horticultural Science, Corvinus University of Budapest 1118 Budapest Menesi str. 44, Hungary article info abstract Article history: Flea beetles (Chrysomelidae, Alticinae) were collected with Pherocon AM yellow sticky traps in maize Received 2 April 2015 plots to compare the assemblages from transgenic Bt- (genetic event MON810, producing Cry1Ab protein Received in revised form effective against lepidopteran pests) and near isogenic maize in Hungary. Altogether, 51,348 flea beetle 7 July 2015 individuals from 26 species were collected. The dominant species were Phyllotreta atra (F.) and Phyllotreta Accepted 8 July 2015 vittula (Redtenbacher). Their abundances along with other (non-P. atra and non-P. vittula) flea beetle Available online 25 July 2015 species showed no significant differences between Bt- and isogenic maize plots. Similarly, no difference was found between Bt maize and isogenic maize plots in the species richness of the flea beetle Keywords: Flea beetles assemblages. © Bt maize 2015 Elsevier Ltd. All rights reserved. MON810 Species composition Phyllotreta atra Phyllotreta vittula 1. Introduction exposed to the Cry1Ab protein, e.g., the Cry1Ab toxin was detected in the flea beetle Chateocnema pulicaria Melsheimer feeding on The Cry1Ab toxin produced by maize hybrids containing MON810 maize (Harwood et al., 2005), although herbivores with MON810 event is highly effective in controlling target Lepidoptera different types of mouthparts (chewing, sucking) may ingest larvae (Ostrinia nubilalis (Hübner), Pyralidae and Sesamia non- different amounts of Bt toxin. Also, predators consuming agrioides (Lefebvre), Noctuidae) and may also affect larvae of other phytophagous insects containing Cry1Ab toxin may move the toxin Lepidoptera species (e.g. Helicoverpa armigera (Hübner) [Eizaguirre into higher trophic levels (Harwood et al., 2005). et al., 2010; Kiss et al., 2003] Mythimna unipuncta (Haworth) European Union legislation requires a pre-market risk assess- [Eizaguirre et al., 2010; Pilcher et al., 1997]). However, maize fields ment of genetically modified crops before commercial use (EC, harbour species rich assemblages of other arthropod groups 2001, 2002; EFSA, 2010; EU, 2013). For that purpose, this study (Mesz aros et al., 1984), including flea beetles, which are present in examined potential effects of genetically modified maize express- maize stands in high numbers, occasionally causing damage in both ing the Cry1Ab toxin on non-target, within-maize herbivores, using Europe (Vor€ os€ and Maros, 2004) and North America (Hoffmann flea beetles as model species. et al., 1995). These phytophagous insects in maize may also serve Several studies have found no differences in abundance, sea- as prey for predacious species (Arpas et al., 2005). The presence of sonal activity and assemblage characteristics in several non-target the Cry1Ab protein in all maize plant parts throughout the whole herbivore taxa in Bt (MON810) and isogenic maize (Balog et al., growing season might affect a number of associated organisms 2010a,b; Bourguet et al., 2002; Daly and Buntin, 2005; Lozzia, besides the target pests. Herbivores feeding on maize may be 1999; Lozzia and Rigamonti, 1998; Musser and Shelton, 2003; Sehnal et al., 2004). These same authors have raised the impor- tance of longer term field studies to detect possible cumulative effects over several seasons, to determine thresholds for detecting * Corresponding author. E-mail address: [email protected] (A. Szen asi). any effects and for selecting suitable species for impact studies. The http://dx.doi.org/10.1016/j.cropro.2015.07.008 0261-2194/© 2015 Elsevier Ltd. All rights reserved. A. Szenasi, V. Marko / Crop Protection 77 (2015) 38e44 39 necessity of a more ecological approach in the study of the potential our study was to complete and supplement these data. impact of growing GM crops on non-target organisms is raised by Cry1Ab protein (MON810 event) shows high specificity to target Andow et al. (2006, 2013), Arpaia et al. (2014), Lovei€ and Arpaia organisms (Ostrinia nubilalis, Sesamia nonagrioides) under labora- (2005), Lovei€ et al. (2009). tory studies (Tier1), and variable mortality to larvae of numerous Several studies have been conducted in Hungary on economi- Lepidoptera species (MON810 SO Update, Perry et al., 2010, 2011) cally important maize pests, secondary pests, other herbivores, and (Tier1a and b, Tier2) and by maize hybrids on the field (Tier3) predators including a 10-year maize ecosystem research study (intended effect). However, only a few in-planta data (unintended (Mesz aros et al., 1984). This faunal survey, however, focused pri- effect) are available about flea beetles in connection with secondary marily on the occurrence of arthropod taxa in the studied maize metabolites and others (Bak et al., 1999; Nielsen et al., 2001; fields and did not collect data on their abundance. Because the Verpoorte and Memelink, 2002). The further purpose of this Cry1Ab toxin is expressed in all maize tissues sampling should study was to survey for possible un-intended effects of the MON810 examine all groups of herbivores in maize that occur at high enough maize on flea beetles. density to permit quantitative comparisons between Bt and isogenic maize. 2. Materials and methods Our study group, flea beetles are best known as pests of Bras- sicaceae crops (Bohinc et al., 2013; Saringer, 1990; Trdan et al., 2.1. Experimental site 2008). In contrast, Phyllotreta vittula (Redtenbacher) has been recorded as a pest on cereals (including maize) (Fritzsche, 1971; The two-year (2002 and 2003) field experiment was carried out Szeoke,} 1997), sugar beet and crucifers (Naibo, 1974), including in an isolated maize stand located near Budapest (GPS, N: 47 250; yellow mustard (Hurej et al., 1997). Vig (1998a) reported a wide E: 18 470), Hungary, surrounded by large stone fruit orchards host range of P. vittula including grasses, maize and Brassicaceae, (apricot, peach and plum). Plots within the experimental field were but damage in Hungary is reported only on cereals, such as maize arranged in a randomized complete block design with six replica- (Nagy and Deseo,} 1969; Szeoke,} 1997). Phyllotreta vittula has been tions. The plots (sized 30 Â 30 m) were planted either with Bt maize found damaging maize in Hungary (Gyulai and Garay, 1996; (DK 440 BTY e transformation event MON810) or with its near Hinfner and Papp, 1961; Jablonowski, 1906; Nagy and Deseo,} isogenic line (DK 440) on chernozem soil. An alley distance of 3 m 1969; Szeoke} et al., 1996; Szeoke,} 1997; Szucs,} 1973; Vor€ os€ and was used between replications. A retention zone (a pollen capture Maros, 2004), in the former Soviet Union (Arnoldi and Gurjeva, crop surrounding the entire test field) was established to a maize 1960; Scsegolev, 1952), in Germany (Sorauer, 1954), in Poland hybrid of similar maturity ground to the test hybrid, in accordance (Kania, 1962), in the former Czechoslovakia (Hruska, 1962), in with the requirements of the release permit. France (Leclant, 1977), in the former Yugoslavia (Sekulic et al., 1989) Maize was planted at a seed rate of 65,000 seeds/ha and was and in Romania (Grozea et al., 2006), making it one of the most reduced to 50,000 plants/ha after emergence. Sowing was in late important Coleoptera species attacking maize foliage (Sekulic et al., April and maize was harvested in mid-October to early November 1989). Leaf-damage by P. vittula is most pregnant in spring on the depending on the year. juvenile plants (Saringer, 1990; Scsegolev, 1951; Szeoke} et al., 1996). In addition to P. vittula, Chaetocnema aridula (Gyllenhal) is found 2.2. Sampling in Hungary on maize and other cereals (Saringer, 1990). The flea beetle Epitrix cucumeris (Harris) is an early season pest of maize in Flea beetle adults were collected with Pherocon AM yellow Kansas, USA, where chemical controls have occasionally been sticky traps (Trece Inc. California, USA), since yellow colour has long needed (Wilde et al., 2004). Chaetocnema pulicaria is a pest of maize been known as attractive for flea beetles (Hung and Hwang, 2000; in the USA (Steffey et al., 1999) and an important pest of sweet corn Vincent and Stewart, 1986). Three traps/plot were placed between in Iowa (Hoffmann et al., 1995). rows 20 and 21, 7.5 m apart and 7.5 m from the field edge. Traps In Hungary, dense flea beetle populations occur only in periods were fixed to a wooden stick at a height of maize canopy until of dry, sunny weather (Saringer, 1990), when young maize plants silking, when they were adjusted to ear height. In 2002, traps were are especially susceptible to injury if drought stressed (Szeoke} et al., changed weekly, and according to the experiences of the first year, 1996; Vor€ os€ and Maros, 2004). In older plants, flea beetles reduce in order to reduce efforts and costs of sampling, in 2003 they were foliar area and thus photosynthesis (Szeoke} et al., 1996). Under dry changed fortnightly. Sampling took place from late May to late conditions, damage increases and plant development is inhibited September in 2002 and from early June to mid-September in 2003. (Nagy and Deseo,} 1969). Among different crops the most conspic- Flea beetle adults were removed by petrol from the traps and uous injury by P. vittula is found in maize, mainly on the edges of submitted to I. Rozner (Museum of Natural History, Budapest) for fields and in unevenly emerged stands. In some cases, the lower identification. Collected adults were identified using the key of 1e4 leaves of certain maize plants are totally destroyed (Gyulai and Warchalowsky (2003).